You would have to do a lot of the stuff manually, rather than using the INDI web interface, that is - you would probably need to start different INDI servers on different TCP ports and then connect different instances of Ekos (perhaps running under different users) to the individual INDI server ports. It would take some planning, but you could get it running.
Where I think you will hit a gotcha, is when you start to download exposures from the multiple cameras, there has long been issues with the available resources when using the bigger cameras e.g. ASI2600 or ASI6200, by having many cameras you are likely to approach those - e.g. USB3 bandwidth & Pi memory constraints, which you are currently avoiding by spreading the load across multiple Pis.
If I were to consider moving everything to a single system, I would probably try to move to a high-spec NUC, and perhaps look for one that had more than 1 USB3 bus on the motherboard, or perhaps a system with a PCIe slot, where I could add an extra USB3 controller (e.g.
www.scan.co.uk/products/4-port-highpoint...-port-plus-uas-boost ). I would probably roll my own system with Ubuntu on that as well, as when you're doing something as custom as that with the system, it is sometimes better to be in full control of the configuration, rather than rely on how someone else has rolled it for a simpler task.
Hope that helps.